Food Partitioning of Leaf-Eating Mangrove Crabs (Sesarminae): Experimental and Stable Isotope (13Cand15n) Evidence
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Estuarine, Coastal and Shelf Science 87 (2010) 583e590 Contents lists available at ScienceDirect Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss Food partitioning of leaf-eating mangrove crabs (Sesarminae): Experimental and stable isotope (13Cand15N) evidence Ditte K. Kristensen a, Erik Kristensen a,*, Perrine Mangion b a Institute of Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark b Vrije Universiteit Brussel, Department of Analytical and Environmental Chemistry, Pleinlaan 2, B-1050 Brussels, Belgium article info abstract Article history: The feasibility of mangrove leaves as a full diet for sesarmid crabs has been questioned for decades. Since Received 18 October 2009 these leaves are nitrogen-poor, sesarmids probably obtain nitrogen from other sources to sustain Accepted 19 February 2010 growth. The aim of this study was to assess the food partitioning of the sesarmid species Neoepisesarma Available online 1 March 2010 versicolor with emphasis on nitrogen allocation. The preference for animal tissue when crabs were pre- fed diets of different nitrogen content was determined in the laboratory. Furthermore, the possible in Keywords: situ diet composition of N. versicolor was established from carbon and nitrogen stable isotope signature Sesarmid crab (d13C and d15N) of freshly caught individuals and their potential food sources, using a concentration- mangrove fi fi food source dependent mixing model. N. versicolor showed signi cantly higher feeding preferences for sh meat stable isotopes when pre-fed leaf material without than with access to meat, indicating that this crab species can meet mixing model its nitrogen demand by ingesting animal tissue. The stable isotope mixing model based on in situ materials suggests that the diet of N. versicolor consists of w60% leaves in terms of biomass, leaving w40% for other sources such as animal tissue and benthic microorganisms. The biomass contribution from animal tissues, in form of e.g. other crustaceans and fish carcasses, was found to account for w15%. Despite the relative low biomass fraction, animal food sources may contribute with up to half of the nitrogen in the diet of N. versicolor. The quantity of ingested sediment most likely exceeds that of animal tissues. However, due to the low concentration of assimilable microalgae and other microorganism, we propose that sediment associated sources are less important as a nitrogen source for N. versicolor than hitherto presumed. Ó 2010 Elsevier Ltd. All rights reserved. 1. Introduction et al., 2002). In addition, the crabs facilitate decomposition of mangrove detritus and recycling of nutrients by macerating and Leaf-eating sesarmid crabs are known to have a high impact on fragmenting the litter through ingestion and gut passage. The crab the mangrove ecosystem in the Indo-West Pacific due to their fecal material consists of macerated and incompletely digested leaf distinctive behavior and feeding ecology (for review, see Lee, 1998 litter, which provides easier access for colonization by bacteria and or Kristensen, 2007). Several studies have shown that these crabs other organisms of the detritus food chain (Kristensen and Pilgaard, consume mangrove leaves as their major food source (e.g. 2001). Robertson, 1986; Steinke et al., 1993; Thongtham and Kristensen, Fresh mangrove leaves are unpalatable to most herbivores 2005), and stomach analyses reveal that leaf fragments account because of their high concentrations of refractory and indigestible for 55e95% of the total content (Malley, 1978; Dahdouh-Guebas polyphenolic compounds, such as tannins. Moreover, due to et al., 1999; Thongtham et al., 2008). Sesarmid crabs primarily a substantial content of cellulose and lignin, the C:N ratio is high consume leaves at the sediment floor or pull them into their compared to plant materials of marine origin. The C:N ratio varies burrows for later ingestion. Hence, they are capable of removing among mangrove species but is in general about 50e100 (e.g. 30e90% of the annual litter production (Robertson, 1986; Micheli, Robertson, 1988; Kristensen et al., 1995). This far exceeds the value 1993b; Slim et al., 1997), reducing tidal exports of mangrove of 17, which is suggested as the maximum for sustainable animal derived organic matter considerably (Slim et al., 1996; Olafsson nutrition (Russell-Hunter, 1970). It has been proposed that the observed preference of sesarmid crabs for partly decomposed leaves is caused by loss of tannins and structural carbon combined * Corresponding author. with enhanced nutritional (i.e. nitrogen) value by microbial colo- E-mail address: [email protected] (E. Kristensen). nization during aging (e.g. Lee, 1989; Robertson and Daniel, 1989; 0272-7714/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2010.02.016 584 D.K. Kristensen et al. / Estuarine, Coastal and Shelf Science 87 (2010) 583e590 Micheli, 1993a). However, this hypothesis has been questioned (e.g. The subfamily Sesarminae is very diverse regarding morphology Skov and Hartnoll, 2002; Thongtham and Kristensen, 2005), and and habitats, though most of the members are semi-terrestrial and even partly degraded mangrove leaves are probably insufficient to associated with mangrove ecosystems. This study focused on the maintain crab growth. This is further corroborated by stable isotope species N. versicolor, which plays an important ecological as well as analyses, which show that sesarmid crabs are more enriched in 13C a socio-economical role in mangrove areas of Thailand (Thongtham than mangrove leaves (Bouillon et al., 2002, 2004). The logical et al., 2008). The aim was to investigate the food partitioning of consequence is that leaf-eating crabs most likely supplement their N. versicolor, with emphasis on nitrogen sources. The hypotheses leaf diet with nitrogen-rich food sources to meet the nitrogen tested were: 1. N. versicolor is capable of supplementing its diet demand. But the origin of these alternative nitrogen sources has with animal tissue; and 2. animal tissue contribute substantially as been and still is under debate. a nitrogen source for N. versicolor. These hypotheses were tested in It is a common opinion in the literature that the majority of leaf- laboratory feeding experiments supplemented with stable isotope eating sesarmid crabs augment their nitrogen supply by ingesting composition analyses of wild caught crabs and their possible food sediment and assimilating the associated microalgae and bacteria sources. The most likely elemental composition and contribution of (e.g. Robertson, 1986; Bouillon et al., 2002; Skov and Hartnoll, animal tissue in the diet were determined by applying a concen- 2002). This is based on the observation that many sesarmid crabs tration-dependent stable isotope mixing model. spend a considerable amount of time feeding on sediment (e.g. Micheli, 1993b; Skov and Hartnoll, 2002; Thongtham et al., 2008). 2. Materials and methods In support of this contention, Bouillon et al. (2002) demonstrated that stable carbon isotope ratios of sesarmids and sediment 2.1. Study area correlate. However, Thongtham and Kristensen (2005) argued that the large sesarmid species, Neoepisesarma versicolor, is physically Individuals of N. versicolor and samples of their potential food unable to consume enough sediment to cover its nitrogen demand. sources were collected in the Bangrong mangrove forest (8 030 N, Along this line of evidence, it has been suggested that some ses- 98 250E) located on the north east coast of Phuket Island, Thailand armid crabs primarily achieve their nitrogen from occasional (Fig. 1). Bangrong is a 2.5 km2 fringe forest receiving no river consumption of animal tissue, such as carcasses of fish, dead and discharges and with the only freshwater supply originating from live crustaceans (Thongtham and Kristensen, 2005; Thongtham direct precipitation and run-off from land. The creek area covers et al., 2008), and small invertebrates associated with the sedi- 0.4 km2 and consists primarily of a 3 km longitudinal main tidal ment floor and leaf litter (Kwok and Lee, 1995). The reliance on channel. Tidal range in the area varies from 1 m at neap tide to 3 m animal tissue is supported by findings of crustacean exoskeleton at spring tide. The climate is monsoonal with a wet season from remains and fish scales in the stomach of N. versicolor (Thongtham May to November and a dry season from December to April. The et al., 2008) and Neosarmatium smithii (Giddins et al., 1986). annual precipitation is about 2300 mm and the average Fig. 1. Map of the Bangrong mangrove forest, Thailand. The two sampling sites are indicated. D.K. Kristensen et al. / Estuarine, Coastal and Shelf Science 87 (2010) 583e590 585 temperature is 28 C. The dominant mangrove species are Rhizo- visible smaller crabs of various species. Green and yellow leaves phora apiculata, Rhizophora mucronata, Ceriops tagal, and Xylocarpus were handpicked from the trees, while brown leaves were granatum. The dominant benthic species are fiddler crabs (familie: collected from the forest floor between trees. Surface sediment Ocypodidae) and sesarmid crabs (family: Grapsidae). (<1 mm) was obtained by careful scraping with a spatula. All samples were transported to the laboratory and immediately 2.2. Neoepisesarma versicolor feeding experiment frozen (À18C). Brown leaves were sorted into two groups before freezing; one was gently rinsed in tap water to remove surface The selectivity